J. Bio. & Env. Sci. 2020

Journal of Biodiversity and Environmental Sciences (JBES) ISSN: 2220-6663 (Print) 2222-3045 (Online) Vol. 17, No. 2, p. 101-112, 2020 http://www.innspub.net

REVIEW PAPER OPEN ACCESS

Insights of allelopathic, insecticidal and repellent potential of an invasive plant Sphaeranthus suaveolens in pest and weed management

Hudson Laizer*1,2, Musa Chacha1, Patrick Ndakidemi1

1Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania 2Centre for Research, Agricultural Advancement, Teaching Excellence and Sustainability in Food and Nutritional Security (CREATES), The Nelson Mandela African Institution of Science and Technology (NM-AIST), Arusha, Tanzania

Article published on August 30, 2020

Key words: Botanical extracts, Secondary metabolites, Sustainable agriculture, Smallholder farmers, Terpene

Abstract Sphaeranthus suaveolens is a weed from the family Asteraceae, it grows abundantly in wet areas and most common in rice fields. The extracts from plants closely related to S. suaveolens have been reported to have allelopathic, insecticidal, antifeedant, repellent, and other biological activities. Currently, the use of synthetic chemicals to control weeds and insect pests raise several concerns related to environment and human health. Extracts from plants with pesticidal properties can offer the best and an environmentally friendly alternative. Some of these extracts have been extensively tested to assess their applications as valuable natural resources in sustainable agriculture. This review article therefore explores the potential of S. suaveolens extracts in controlling insect pests and managing weeds by smallholder farmers.

*Corresponding Author: Hudson Laizer  [email protected]

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potential. S. suaveolens is a widespread weed in Introduction swampy and irrigated farmlands, and usually infests Agricultural production in most part of the world is cultivated fields and reduces crop productivity affected by pests, diseases and weeds among other (Beentje, 2002). A heavy infestation of this weed factors (Nations, 2016; Singh et al., 2003). Majority results in adverse effects on the growth and yield of of the farmers respond to these constraints through crops, particularly in rice fields (Fahmy, 1997). the use of synthetic chemicals such as herbicides and pesticide (Kelly et al., 2003). The extensive use of It has been observed that S. suaveolens has an ability these chemicals in controlling insect pests and to overcome and suppress crop plants in a wide range managing weeds, however, have alarmed the public over a short period of time (Ivens, 1989). However, on the effects they might bring to human health and the secondary metabolites involved are largely the environment at large (Khanh et al., 2005). Such unknown and weather they can be applied in concerns are putting pressure on agricultural sector managing other weeds and controlling insect pests is to reduce the use of chemicals and as a result, much yet to be determined. Understanding this could attention is paid to alternative methods and considerably justify the practical application of techniques for controlling and managing weeds and botanical-based weeds and insect pests management insect pests, through non-chemical methods and/or techniques for most smallholder farmers in areas use of natural products such as botanical extracts where S. suaveolens is growing. (Isman, 2006a; Williamson et al., 2008). This review article therefore highlights the Prior to the discovery and commercialization of allelopathic, insecticidal and repellent potential of an synthetic pesticides, botanical extracts, among other invasive plant S. suaveolens with a focus on its methods, were used by most farmers in crop application in controlling insect pests and managing protection against insect pests, weeds and diseases weeds by smallholder farmers. (El-Wakeil, 2013). Extracts from plants with allelopathic or pesticidal properties were of great Overview of S. suaveolens and its spatial distribution importance in making natural herbicides and in Tanzania pesticides (Benner, 1993; Godfrey, 1994). There is S. suaveolens is an aromatic annual spreading herb also increasingly evidence from literatures that plant from the family Asteraceae with broad sessile leaves extracts can be manipulated and used as perfect covered with glandular hairs (Osman, 2011). The lower agrochemicals in controlling insect pests and stem often trails along the ground and roots at the managing weeds (Hoagland, 2001; Macías et al., nodes with thread-like root, flowers are purple, in 2001; Mkenda et al., 2015; Nattudurai et al., 2012; compound heads ovoid in shape and borne on solitary Ngondya et al., 2016; Singh et al., 2003; Stephen et glandular peduncles with toothed wings (Fayed & al., 2002; Vyvyan, 2002). Mohamed, 1991).

The secondary metabolites in plants are responsible The head as a whole is surrounded by several rows of to biological activities that offer defense against bracts, of which only the tips are visible when flowers predators, fungi and bacteria, also these metabolites are fully open, and propagated by seeds which takes may act as natural herbicides by suppressing other about 10-12 days to germinate, and the seedlings attain plant species (Dewick, 2009; Schoonhoven et al., the height of 5.0 - 6.0cm within 30 days in a favorable 2005). These biological activities from the plants environment (Beentje, 2002). secondary metabolites can be exploited and manipulated for various human uses, and in this S. suaveolens is widespread in Africa over a range of respect Sphaeranthus suaveolens has a considerable altitudes from Rwanda, Burundi, Sudan, Ethiopia,

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Zambia, Malawi, Mozambique, Egypt, Uganda, Kenya then Mpwapwa (Launert, 2003), Mkata and Mandela to Tanzania (Everard et al., 2002; Fahmy, 1997). It is in Wami River Ecosystem (Mligo, 2017). The spatial mostly found growing in wet areas and thrives well in distribution of S. suaveolens in Northern Tanzania medium clayey soils, but also common in and around particularly Arusha and Kilimanjaro regions however, irrigation ditches and rice fields and considered as a have not been mapped despite being reported as a major weed in most farms (Ivens, 1989). In Tanzania, weed to most agricultural fields. the plant was first reported in Songea (Brenan, 1960),

Fig. 1. Distribution of S. suaveolens in Wami River Ecosystem in Tanzania.

Allelopathic effects of S. suaveolens on crops & Leather, 1988). Allelopathy is a phenomenon, whereby one plant Most allelopathic plants have been observed to influences the growth of another one, including significantly affect the growth, productivity and yield microorganisms by the release of chemical of other crops by causing soil sickness and nutrient compounds into the environment (Keeley, 2010; Rice, imbalance (Kohli et al., 2008), as well as affecting the 1983; Whittaker & Feeny, 1971). The allelopathic microbial population (Batish et al., 2001). Several effects are the result of chemical compounds known studies have indicated that, most weeds possess as allelochemicals, which are usually plants’ allelopathic effects which play a significant roles in secondary metabolites or byproducts of the principal their invasion success (Macías et al., 2014; Qasem & metabolic pathways in plants (Chancellor, 1987; Foy, 2001; Zhou et al., 2013). Numerous weeds from Dayan et al., 2009; Macías et al., 2007). In recent the Asteraceae family have been reported to possess years, allelopathy has become a research hotspot for allelopathy and can significantly inhibit crop making comprehensive analysis about the mechanism productivity in agricultural land (Ilori et al., 2010; of weeds and identification of specific chemical Kong et al., 2007). The invasive weed, Sphaeranthus compounds responsible for allelopathic effects indicus has been reported to inhibit seed germination (Azirak & Karaman, 2008; Bais et al., 2003; Einhellig and growth of wheat (Triticum aestivum), rice (Oryza

103 | Laizer et al. J. Bio. & Env. Sci. 2020 sativa) and mung bean (Vigna radiata) in different effects to the environment and human health farming systems (Lodha, 2004). (Ferguson et al., 2009). Recently, Mahajan et al. (2015) reviewed the The allelopathic potential of S. suaveolens, therefore allelopathic potential of S. indicus and found that the need to be realized and selectively used to suppress germination and seedling growth of various crops density of other weeds and insect pests population were significantly decreased with increase in particularly in small farming agricultural systems. concentration of its extract. Insecticidal and repellent activities of S. suaveolens Despite of the negative effects on cultivated crops, to insect pests allelochemicals from allelopathic plants can be Insecticides, weather natural or synthetic are manipulated and used to control weeds of various developed to either kill, repel, or interfere with the crops. For example, Khanh et al. (2006) noted that damaging behavior of insect pests (EPA, 2009). Due the allelochemicals contained in tissues of Passiflora to intensity of plant-insect interactions, plants have edulis can significantly suppress the two noxious well developed defense mechanisms against insect paddy rice weeds (Echinochloa crusgalli and pests by producing natural compounds which acts as Monochoria vaginalis). Other studies have also natural pesticides (Després et al., 2007). The most reported the use of allelochemicals for weed control in exciting concept is to isolate and identify such the laboratory as well as application under field compounds and use them as candidates in making conditions (Jabran et al., 2015; Ngondya et al., 2016). safer pesticides (Maia & Moore, 2011). Plant extracts Jamil et al. (2009) described the utilization of with pesticidal properties can be active against allelopathic water extract as an important and useful specific target insects, biodegradable, have low to way of exploiting the allelopathic potential to manage non-toxic effects, cheap and easy to prepare (Kim et wild oat and canary grass in wheat fields. al., 2003; Mkindi et al., 2017). Due to this facts, these

plant extracts could lead to the development of new The emergence and root length of most rice weeds classes of safer pesticides (Céspedes et al., 2014; was inhibited by allelochemical (Lycorine) from the Tembo et al., 2018). dead leaves of spider lily (Iqbal et al., 2006). The allelopathic crops when used as cover crop, mulch, The Asteraceae family in which S. suaveolens belongs, smother crops, green manures, or grown in rotational have been reported to contain plants with insecticidal sequences maybe helpful in reducing noxious weeds activities (Dhale, 2013; Green et al., 2017; Sosa et al., and plant pathogen, improve soil quality and crop 2018). These insecticidal activities are mostly linked yield (Khanh et al., 2005). to presence of secondary metabolites such as Furthermore, the application of allelopathic extracts terpenes, which can act as larvicides, insect growth may give an efficient alternative control over weeds regulators and feeding and oviposition deterrents similar to that offered by synthetic herbicides (Xuan (Miresmailli & Isman, 2014). Terpene is among the et al., 2004). Interactions among potential most diverse class of plant secondary metabolites allelopathic plants, target pests and other non- target found in essential oils of most plants, S. suaveolens organisms in a cropping system also need to be included (Ahmed et al., 2017; Pagare et al., 2015). considered and fully realized to avoid detrimental This secondary metabolite has been reported to play effects to desired crops and non-target species an important role in plant protection against (Farooq et al., 2013). pathogens (Neerman, 2003), insects (Wu et al., 2016) and toxic to mammals as well (Gurib-Fakim, 2006). The allelochemicals involved in weed suppression can Recently, Sosa et al. (2018) reported insecticidal serve as basic templates for developing new activities of the terpene isolated from Vernonanthura generation of biopesticides with low or no toxic nebularum against fall army warm (Spodoptera

104 | Laizer et al. J. Bio. & Env. Sci. 2020 frugiperda) and fruit fly (Ceratitis capitate). biological activities such as antimicrobial, immune stimulating, anticancer, antitumor, anthelmintic, Moreover, two other terpenes from Inula helenium repellency, insecticidal and allelopathy (Ahmed & were examined by Kaur et al. (2017) and reported to Mahmoud, 1997; Kleinowski et al., 2016). However, significantly inhibit the growth of tobacco leafworm very few literatures have reported the identified (Spodoptera litura). compounds found in S. suaveolens extracts, none of it has a list of allelochemicals found in S. suaveolens Other techniques such as use of water extracts from S. despite being the weed of economic importance in indicus was also reported to demonstrated toxic many rice and common bean farms in Africa. effects against insect pests such as rice weevil (Patole et al., 2008), cowpea weevil (Singh & Shrivastava, Allelochemicals belong to various chemical groups, 2012) and red flour beetle (Pugazhvendan et al., and can be classified based on their structures and 2012). Furthermore, the extracts from S. indicus have properties into: water-soluble organic acids, straight- been showing larvicidal activities and repellent chain alcohols, aliphatic aldehydes, and ketones, activities to most of the insect pests (Arivoli et al., lactones, long-chain fatty acids and polyacetylenes, 2016; Baby, 1994; Singh & Shrivastava, 2012). quinines (benzoquinone, anthraquinone and complex quinines), phenolics, cinnamic acid and its The presence of secondary metabolites with pesticidal derivatives, coumarins, flavonoids, tannins, steroids properties such as terpene in the essential oil of S. and terpenoids (Li et al., 2010). suaveolens may give positive insecticidal and repellent activities to most insect pests, hence used Most of these biochemicals are synthesized during the for as protective agents against insect pests, but this shikimate pathway (Hussain & Reigosa, 2011) or, in needs further scientific investigation. the case of essential oils, from the isoprenoid pathway (Rehman et al., 2016). The extract of the aerial parts Key allelochemicals from the leaf, stem and root of S. suavealens was reported by Jakupovic et al. extracts of S. suaveolens (1990) to contain eight eudesman-12. 6 β abides, Allelochemicals are secondary metabolites produced carvotacetone derivatives and a thymohydroquinone by living organisms such as plants that have glucopyranoside. Later on, Pooter et al. (1991) stimulatory or inhibitory effects upon the growth, reported extract of the same plant comprise of health, behavior and distribution of neighboring thymohydroquinone dimethylether, a diacetylene organisms being another plants, insects or microbes thiophene, inositol and myoinositol esters, and (Haig, 2008). The role played by secondary several carvotanacetone derivatives, he went further to metabolites is mostly ecological, linked to plant examine the essential oil of S. suaveolens and noted defense against other plants, pests, or diseases methyl chavicol, α-ionon,e, dcadinene and p- (Ramakrishna & Ravishankar, 2011). Allelochemicals methoxycinnamadehyde as major constituents, and a- undoubtedly pose problems in agriculture, but if well terpinene, citral, geraniol, geranyl acetate, βionone, manipulated they can be beneficial and offer great shaerene, indicusene and sphaeranthol as minor opportunities such as insect pests and weeds control constituents. Ahmed and Mahmoud (1997) examine (Einhellig, 1987). Despite the efforts in allelopathic the extract of aerial parts of S. suaveolens and reported researches, little is known on the potential to exploit three carvotacetone derivatives, together with four the key allelochemicals in agricultural systems and monoteroene compounds. Later on, Hassanali et al. use them as templates in making safer and affordable (1998) reported cis-pinocamphone as the major herbicides and/or pesticides (Kremer & Ben- constituents (63.5%) of the leaf oil of S. sauveolens. Hammouda, 2009). Much of the work to date has focused on weather extracts from S. suaveolens show The details of these identified compounds are stated

105 | Laizer et al. J. Bio. & Env. Sci. 2020 in Table 1, however, identifying alone isn’t sufficient individual farmer's resources, including knowledge enough, rather gaining an understanding on which and farming practices (Ikerd, 1993). Unfortunately, among these compounds are allelochemicals and how most smallholder farmers in developing countries to use them in improving crop production though have limited knowledge and are resource- managing weeds and controlling insect pests in constrained. This limits their capacity to manage sustainable agriculture will be a big advantage. weeds and insect pests (Whitbread et al., 2010).

Table 1. Identified compounds from leaf oil of S. Pest management practices by most smallholder suaveolens. farmers are mainly based on use of chemical Compound Ip on RSL-150 Content pesticides, though this alone does not give the desired results (Toda & Morishita, 2009). Few of these α- Thujene 921 0.1 α- Pinene 931 10.6 farmers have combined such method with some Camphene 941 0.1 cultural practices such as intercropping and crop Sabinene 964 1.5 Oct-1-en-3-ol 967 0.3 rotation (Ajeigbe et al., 2010; Ngowi et al., 2007). Myrcene 981 0.6 Other studies reported that limited technical α- Phellandrene 995 4.1 α- Terpinene 1007 tr knowledge among small holder famers and shortage p- Cymene 1011 6.3 of extension services are among the limiting factors 1,8- Cineole 1019 6.6 γ- Terpinene 1049 1.1 that hinder the adoption of suitable pest management trans- Pinene hydrate (?) 1131 0.3 practices (Midega et al., 2012; Mkenda et al., 2020). Pinocamphone 1139 1.0 Isopinocamphone 1155 33.5 Most farmers still relying on past experience and Terpinen-4-ol 1164 0.7 farming practices despite the fact that they have not p- Cymen-8-ol 1170 0.4 α-Terpineol 1173 0.6 attained fruitful results over the years (Khan & Methyl thymol ether (?) 1222 0.1 Damalas, 2015). Integrating different pest Cuminaldehyde 1228 tr Thymol 1267 0.2 management practices has long been proposed as the Carvacrol 1274 0.3 long term solution and future for sustainable α- Terpinyl acetate 1329 1.2 Eugenol 1330 tr agriculture (Pretty & Bharucha, 2015). α- Ylangene 1369 tr β- Elemene 1382 tr For any pest management approach to work and Thymohydroquinone 1400 16.1 dimethylether 1418 0.9 eventually adopted by farmers, their knowledge, β- Caryophyllene 1447 0.1 perceptions and practices has to be fully realized α- Humulene 1449 0.1 β-Farnesene 1461 tr (Chitere & Omolo, 2008; Hashemi & Damalas, 2010; allo- Aromadendrene 1515 1.2 Huis, 2014). Khan et al. reported that some farmers are δ- Cadinene 1547 0.1 Nerolidol 1564 0.7 aware of the role played by companion crops with Spathulenol 1570 0.4 repellent or toxic characteristics in pests control, as well Caryophyllene oxide tr = trace (<0.05%); (?) = identification based on the as harboring natural enemies and in this regard, S. MS and RT suaveolens may have considerable potential (Khan et al., Source: Pooter et al. (1991) 2010). Isman and Grieneisen (2014) pointed out several plant species from the Asteraceae and other families Farmers knowledge and perception towards use of S. with pesticidal properties that may be used to control suaveolens in insect pests and weeds management and manage insect pests and weeds, however, very few The diversity of insect pests and weeds in most of these plants are known and used by smallholder agricultural lands need a multi-control strategies to farmers despite the increasingly focus in research on produce satisfactory results in a sustainable manner plant species with pesticidal potential in Africa. (Parker et al., 2013). The goals and values of long- term sustainability must be reflected in combinations Conclusion of practices and methods consistent with an

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